Colonisation resistance in the sand fly gut: Leishmania protects Lutzomyia longipalpis from bacterial infection

Abstract

BackgroundPhlebotomine sand flies transmit the haemoflagellate Leishmania, the causative agent of human leishmaniasis. The Leishmania promastigotes are confined to the gut lumen and are exposed to the gut microbiota within female sand flies. Here we study the colonisation resistance of yeast and bacteria in preventing the establishment of a Leishmania population in sand flies and the ability of Leishmania to provide colonisation resistance towards the insect bacterial pathogen Serratia marcescens that is also pathogenic towards Leishmania.MethodsWe isolated microorganisms from wild-caught and laboratory-reared female Lutzomyia longipalpis, identified as Pseudozyma sp. Asaia sp. and Ochrobactrum intermedium. We fed the females with a sugar meal containing the microorganisms and then subsequently fed them with a bloodmeal containing Leishmania mexicana and recorded the development of the Leishmania population. Further experiments examined the effect of first colonising the sand fly gut with L. mexicana followed by feeding with, Serratia marcescens, an insect bacterial pathogen. The mortality of the flies due to S. marcescens was recorded in the presence and absence of Leishmania.ResultsThere was a reduction in the number of flies harbouring a Leishmania population that had been pre-fed with Pseudozyma sp. and Asaia sp. or O. intermedium. Experiments in which L. mexicana colonised the sand fly gut prior to being fed an insect bacterial pathogen, Serratia marcescens, showed that the survival of flies with a Leishmania infection was significantly higher compared to flies without Leishmania infection.ConclusionsThe yeast and bacterial colonisation experiments show that the presence of sand fly gut microorganisms reduce the potential for Leishmania to establish within the sand fly vector. Sand flies infected with Leishmania were able to survive an attack by the bacterial pathogen that would have killed the insect and we concluded that Leishmania may benefit its insect host whilst increasing the potential to establish itself in the sand fly vector. We suggest that the increased ability of the sand fly to withstand a bacterial entomopathogen, due to the presence of the Leishmania, may provide an evolutionary pressure for the maintenance of the Leishmania-vector association.Electronic supplementary materialThe online version of this article (doi:10.1186/1756-3305-7-329) contains supplementary material, which is available to authorized users.

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

“…Recent evidence is mounting that the transmission of vector‐borne pathogens can be inhibited by other vector‐associated microbes (Sinkins, 2013). In the past decade, studies have shown that certain microbes associated with insect vectors could be used to mediate the transmission of diseases including those transmitted by mosquitoes (Capone et al., 2013; Cirimotich et al., 2011; Dong, Manfredini, & Dimopoulos, 2009; Mourya, Pidiyar, Patole, Gokhale, & Shouche, 2002; Ramirez et al., 2014; Tchioffo et al., 2013; Xi, Ramirez, & Dimopoulos, 2008), tsetse flies (Pais, Lohs, Wu, Wang, & Aksoy, 2008; Wang, Wu, Yang, & Aksoy, 2009; Weiss, Wang, Maltz, Wu, & Aksoy, 2013), sand flies (Sant'Anna et al., 2014), and ticks (Gall et al., 2016; Narasimhan et al., 2014). The most striking example is the inhibition by bacterium Wolbachia pipientis of virus and parasite infection in mosquito vectors (Bian, Xu, Lu, Xie, & Xi, 2010; Blagrove, Arias‐Goeta, Di Genua, Failloux, & Sinkins, 2013; Frentiu et al., 2014; van den Hurk et al., 2012; Hussain et al., 2012; Moreira et al., 2009).…”

Diversity of bacteriome associated with Phlebotomus chinensis (Diptera: Psychodidae) sand flies in two wild populations from China

“…Regarding the microbial contributions to the physiology of sand flies, gut bacteria have been shown to play roles in development17 and immunity1819. In addition, evidence has become available that resident microorganisms in the gut are able to inhibit Leishmania infections2021.…”

Screening of Fungi for Biological Control of a Triatomine Vector of Chagas Disease: Temperature and Trypanosome Infection as Factors

“…A particularly relevant study is one in which the sand fly Lutzomyia longipalpis infected with the pathogenic bacterium Serratia mercescens was shown to survive longer when parasitized with Leishmania mexicana than without the parasite [34]. Those authors propose a mutualism between the insect vector and L .…”